Making different sentences out of the same words was thought to be a unique feature of human language but scientists have now discovered syntax in monkeys.
A study of wild putty-nosed monkeys in Africa has found that they can mix different alarm calls to communicate new meanings to fellow members of a troop.
Scientists found that the two basic sounds - ''pyows'' and ''hacks'' - which are used to warn against different predators can be combined to mean something quite different. The monkeys call out ''pyows'' to warn against a loitering leopard and ''hacks'' are used to warn about hovering eagles overhead. However, combining pyow and hack means something like ''let's go'', according to scientists from the University of St Andrew's.
''To our knowledge, this is the first good evidence of syntax-like natural communication system in a non-human species,'' said Klaus Zuberbühler, one of the researchers.
The putty-nosed monkeys in the study live in the Gashaka Gumti National Park in Nigeria and were frequently heard using different sounds in response to different threats. Kate Arnold, the other member of the team, said that she became aware that the monkeys used several ''pyows'' followed by a few ''hacks'' as a way of telling a group to move away to safer terrain.
''These calls were not produced randomly and a number of distinct patterns emerged. One of these patterns was what we have termed a ''pyow-hack sequence'. This sequence was either produced alone or inserted at certain positions in the call series,'' Dr Arnold said.
''Observationally and experimentally we have demonstrated that this call sequence serves to elicit group movement in both predatory contexts and during normal day-to-day activities such as finding food sources,'' she said.
The scientists demonstrated in a study published in Nature that they would imitate the communication syntax of the monkeys by playing recorded calls to the wild troop living in the forest.
''The pyow-hack sequence means something like 'let's go' whereas the pyows by themselves have multiple functions and the hacks are generally used as alarm calls,'' Dr Arnold said.
''Previously, animal communication systems were considered to lack examples in which call combinations carried meanings that were different to the sum of the meanings of the constituent elements,'' she said.
''This is the first good example of calls being combined in meaningful ways. The implications of this research are that primates, at least, may be able to ignore the usual relationship between an individual call and any meaning that it might convey under certain circumstances,'' Dr Arnold added.
Sounding off: how animals communicate
* DOLPHINS
While it is not known whether dolphins have a formal language, they do have a signature whistle to identify themselves. Though they lack vocal chords, their sphincter muscles produce a complicated series of moans, trills and clicks. When a dolphin sees an object in the distance, particularly in murky water, it emits clicking sounds and listens to the echo to identify distance and object size.
* BIRDS
Bird calls are used to express alarm, and to keep members of a flock in contact, whereas songs which mainly come from male birds are used to claim territory or advertise for a mate. Basic song is the same for all members of a species, and it is believed that young birds learn the details of songs from their fathers. As variations build up over generations, they form a dialect. In a 2005 study in Science, it was shown that the number of "dees" in a chick-a-dee call corresponds to the degree of danger that a predator poses.
* WHALES
Whales communicate and navigate through sound. The best-known whale communication is the song performed by male humpback whales during the mating season. The song is believed to be part of sexual selection, but whether the songs are "flirting" from male to female, competitive behaviour between males or a means of marking territory is still the subject of research.
* FROGS
Frogs have a complex system of calls, the most notable when they have returned to the body of water where they were born. The male frog then uses calls to attract a mate, either by themselves, or collectively as a chorus. In some species of frog, including Polypedates leucomystax, the female frog will reply to the call. If mounted by another male, the frog emits a release call. Tropical species use a callto signal the start of rain. The only call the frog makes with its mouth open is the high-pitched distress call.
Geneviève Roberts
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